Responses to commentaries by Finch, Nilsson et al., Abrams, and Schaie

advertisement
Neurobiology of Aging 30 (2009) 530–533
Author’s response to commentaries
Responses to commentaries by Finch, Nilsson et al.,
Abrams, and Schaie
Timothy A. Salthouse ∗
Department of Psychology, University of Virginia, 102 Gilmer Hall, P.O. Box 400400, Charlottesville, VA 22904-4400, United States
Received 29 December 2008; accepted 1 January 2009
Available online 23 February 2009
I appreciate the interest of the commentators in my article,
and I welcome the opportunity to respond to their comments.
I have admired Caleb Finch’s work on the neurobiology
of aging for many years, and therefore I was pleased to see
that he supports my general conclusion that some cognitive
changes likely begin in early adulthood. As he mentions in
his commentary, he has long advocated research focusing on
the entire period of adulthood instead of merely on groups at
the extremes, and he briefly summarizes some of his excellent
research documenting age differences in various aspects of
neurobiology in his commentary. I also agree with his point
that the next phase of research should address causal linkages
between cognitive aging changes and changes in brain structure and metabolism. This will likely require communication
and interaction among researchers who primarily focus on
age-related changes in cognitive abilities and those who primarily focus on neurobiological measures of brain structure
and function, and his commentary may signal the beginning
of this type of endeavor.
Abrams raised three particularly relevant points in her
commentary. In her first point she noted the existence of other
cognitive variables in which cross-sectional differences are
apparent in middle age. I suspect that this is likely true for
most variables in which extreme group comparisons have
revealed age differences because it seems implausible that
age-related differences occur abruptly immediately before
the age of the older groups.
The second point concerns the existence of variation in
the results across variables. As I noted in the target article,
the estimates of the retest effects are somewhat noisy, but it
is nevertheless important to recognize that there is also considerable consistency in that all 12 variables had negative
∗
Tel.: +1 434 982 6323.
E-mail address: salthouse@virginia.edu.
0197-4580/$ – see front matter © 2009 Elsevier Inc. All rights reserved.
doi:10.1016/j.neurobiolaging.2009.01.004
cross-sectional age trends whereas 8 had positive longitudinal age trends, all 12 had positive short-term retest estimates,
10 of 12 had positive retest estimates from the twice-versusonce tested contrast, and 10 of 12 had positive retest estimates
from the method based on variable retests. Finally, in comparisons of the retest estimate with the longitudinal change,
the retest estimate was larger in 11 of 12 comparisons with
short-term retests, larger in all 12 comparisons with retest
estimates based on the twice-versus-once test, and larger in 8
of 12 comparisons with the estimate derived from the mixed
effects model. Regardless of the amount of variability in the
patterns of results, however, it is clear that better understanding is needed of the nature of cognitive change, including the
relative contributions of retest and other influences.
Abrams’ third point was that researchers need to be cautious in interpreting results based on the use of participant
pools in which the same individuals serve in multiple studies. I particularly liked her phrase “inadvertent retesting”,
because I believe the influence of different types of testing experience on subsequent performance is an important
unresolved question.
In their commentary Nilsson and colleagues note several
disagreements with my target article, and in fact, based on
the description of the article in their abstract and in other
places in their commentary, I also disagree. For example, I
am not comfortable with claims that longitudinal data should
be “dismissed,” and “should not be trusted because they are
flawed,” that “cross-sectional data are to be preferred,” and
that “cognitive function is a homogeneous and unitary entity.”
Because these authors apparently found the article
confusing, it may be useful to briefly restate the major
arguments. The impetus for the article was the striking
discrepancy between the age trends in some measures of
cognitive functioning revealed from cross-sectional and longitudinal comparisons, particularly before age 60. As noted
T.A. Salthouse / Neurobiology of Aging 30 (2009) 530–533
in the article, the discrepancy is not apparent with measures
of knowledge such as crystallized intellectual ability or
semantic memory, and thus they were not considered relevant
to the question of when cognitive decline begins. This does
not mean that aspects of knowledge and information are
not an important part of aging cognition, but the neglect
merely reflects the fact that these aspects do not exhibit the
phenomenon of primary interest in the target article.
Two major interpretations of the discrepancy have been
proposed. One is that cross-sectional comparisons are confounded by cohort differences, such that people of different
ages also differ in other respects that might contribute to
different levels of performance. The second interpretation
is that longitudinal comparisons are confounded by retest
effects, such that performance on the second occasion reflects
influences of age and of prior testing experience. Other
possibilities could obviously be operating as well, but the
focus in the target article was on these two alternatives, and
whether they could be distinguished by determining if the
age trends were altered by eliminating the critical confounding.
The argument with respect to the cohort interpretation was
that if cohort is a meaningful concept, then it should be possible to quantify its characteristics and examine their influence.
Specifically, people of different ages should vary in the relevant cohort-defining characteristics, and these characteristics
should be related to measures of cognitive performance. Furthermore, a primary implication of the cohort interpretation
is that if the variation in these characteristics were statistically controlled, the age differences in relevant measures of
cognitive performance should be greatly reduced. Although
seemingly straightforward, the problem with this strategy is
that it has been difficult to identify and quantify presumably
relevant cohort characteristics such as quality of education,
child-rearing practices, or impact of the media on the individual. One approach to the problem is to accept that critical
dimensions of cohort are not yet measurable, and hence that
the concept is not currently amenable to scientific investigation. However, a more productive alternative is to examine
characteristics that are quantifiable, such as amount of education, aspects of physical and mental health status that reflect
medical advances, sensory abilities, etc. These measures are
unlikely to reflect all aspects of what is meant by the cohort
concept, but they nevertheless serve as a beginning for investigation of the concept.
The study reported in the target article statistically controlled amount of education as well as various indicators
of physical and mental health status, and found large crosssectional age trends in several different measures of cognitive
functioning between 18 and 60 years of age. The conclusion was that cohort influences, at least as measured by those
particular characteristics, cannot account for all of the crosssectional age trends in cognitive functioning. It is important
to emphasize that this does not mean that cohort differences
do not exist and might not be contributing to cross-sectional
age differences in cognitive functioning, but rather that con-
531
trol of the indicators that have been investigated thus far has
not resulted in the elimination of the age differences.
Two other observations were also mentioned that appear
inconsistent with the cohort interpretation. One is that the discrepancy between longitudinal and cross-sectional age trends
is apparent over intervals as short as 7 years (Schaie), 5 years
(Ronnlund et al.) or 2.5 years (current project). These results
imply that if cross-sectional declines are attributable to cohort
differences, then the cohort influences must operate over very
short intervals, and not merely over periods of generations
as sometimes assumed. The second observation is that crosssectional age trends in measures of cognitive functioning have
been reported in non-human animals raised in constant environments in which little or no cohort influences are likely to
be operating.
In order to investigate retest confounds in longitudinal
comparisons the hypothesized retest component in longitudinal change must be distinguished from other determinants
of change. In my opinion no consensus is currently available regarding the best method for estimating retest effects.
Instead of relying on a single method, therefore, I examined
multiple methods, involving short-term retest influences, performance of individuals tested twice versus those tested once,
and a statistical model capitalizing on variability of the retest
intervals. Furthermore, rather than assuming that cognitive
functioning was unitary, 12 different variables selected to
represent 4 different cognitive abilities were examined with
each method. As noted above, there was considerable variability in the absolute magnitudes of the retest estimates.
However, most of the estimates of the retest effects were
positive, which is consistent with the view that measures of
longitudinal change reflect a mixture of influences, and that
positive retest effects may be obscuring maturational decline
occurring prior to about age 60.
Because the results revealed that the cross-sectional
declines were not eliminated after adjusting for variations
in characteristics that might be assumed to reflect cohort
differences, but that the longitudinal age trends were likely
distorted by the presence of positive retest effects, it was
concluded that at least some of the discrepancy between
cross-sectional and longitudinal age trends is probably
attributable to the presence of retest effects masking declines
in longitudinal comparisons.
Schaie raised a number of issues in his commentary, and
with the exception of those that seem to reflect his personal
preferences (e.g., the nature of the citations and the format
of data presentation), each will be addressed in the following
paragraphs.
A major objection appears to be that I am “reifying the
cross-sectional fallacy”. I believe that this is a distorted characterization because my primary proposal is that researchers
need to be careful in the interpretation of both cross-sectional
and longitudinal data. Indeed, one of the final statements
in the target article was that “strengths and weaknesses of
both cross-sectional and longitudinal data . . . need to be
considered when reaching conclusions about age trends in
532
T.A. Salthouse / Neurobiology of Aging 30 (2009) 530–533
cognitive functioning”. From my perspective, therefore, the
most relevant fallacy may be the one I am trying to challenge,
namely, the “single cause fallacy” of interpreting either crosssectional or longitudinal data as a reflection of only a single
type of influence. My guiding assumption was that both crosssectional and longitudinal comparisons are likely influenced
by multiple factors, and that researchers should try to identify
and quantify those factors to investigate their relative contributions to the observed differences and changes. As Schaie
points out, some version of the “cohort hypothesis” has been
discussed for many years, but surprisingly little research has
attempted to investigate the hypothesis by determining the
specific variables that differ across birth cohorts, determining whether those variables are related to the measures of
cognitive functioning which exhibit discrepancies between
cross-sectional and longitudinal age trends, and determining
if the cross-sectional age differences in those cognitive measures are reduced after statistically controlling the variation
in those measures. Rather than accepting cohort and retest
confounds as intrinsic and inevitable, and thereby reifying
any particular assertion, my proposal was that the various
determinants should be identified, quantified, and directly
investigated.
It is indisputable that there have been generational
increases in the average level of performance on some cognitive tests (i.e., the “Flynn Effect”), but the reasons for this
phenomenon, and its implications for the interpretation of age
trends in cognitive functioning, are still not well understood.
In a recent monograph, I (Salthouse, in press) suggested that
these historical increases in average level of performance
should not necessarily be equated with cohort influences
because the increases could reflect period influences, and
might actually have greater distorting influences on longitudinal comparisons than on cross-sectional comparisons. That
is, in a manner similar to how the existence of time-related
inflation changes create greater complications in longitudinal
contrasts of relations between age and salary than in crosssectional contrasts, historical increases in average level of
cognitive functioning could distort longitudinal comparisons
more than cross-sectional comparisons. Until there is better
understanding of the causes and consequences of generational differences in cognitive performance, therefore, it may
be misleading to equate them with cohort differences, and
to assume that they necessarily lead to confounds only in
cross-sectional comparisons.
Schaie also questions the relevance of animal and neurobiological results to this type of research. I am frankly puzzled
by the suggestion that results with non-human animals and
with neurobiological variables might not be relevant to the
question of when age-related cognitive decline begins. In fact,
I believe that the neglect of the vast literature on animal cognition, and until recently also the literature on neurobiological
variables, within the area of cognitive aging has led to a narrow, and possibly distorted, view of the nature of age-related
differences and changes in cognition. As mentioned in the
target article, I believe there are several reasons this litera-
ture is relevant to the current topic. First, as Schaie notes,
congruence of age differences and age changes might be
expected under conditions of stable environments. The existence of many reports of cross-sectional age differences in
measures of memory and cognition in species from primates
to fruit flies raised in nearly constant environments is therefore clearly relevant to the interpretation of cross-sectional
data because these results suggest that age differences can
occur even in the absence of environmental changes. And
second, if retest effects distort longitudinal comparisons,
then a discrepancy between cross-sectional and longitudinal age relations would be expected in non-human animals
with measures of behavior that are susceptible to practice
improvements, but no discrepancy would be expected with
neurobiological variables, such as measures of brain volume,
that are not susceptible to practice effects. As reported in the
target article, research has supported both of these expectations, and thus these results are more consistent with the
retest interpretation of the longitudinal – cross-sectional discrepancy than the cohort interpretation.
Schaie also claims that I do not pay sufficient attention to
domains that remain stable. As noted earlier in this response,
and in the target article, domains that remain stable are not
directly relevant to question of discrepancy between crosssectional and longitudinal because they do not exhibit the
discrepancy.
Another objection is that I dismiss “well-established
effects of cohort differences in providing the major cause
for discrepancies between cross-sectional age differences
and longitudinal age changes.” Instead of dismissing the
cohort hypothesis as a possible explanation of the discrepancy, I actually attempted to investigate it, along with a
plausible alternative hypothesis that postulates that retest
effects distort longitudinal changes. Because Schaie does
not mention what variables should be controlled in order
to adequately control for cohort differences, and because
few explicit characteristics other than education have been
mentioned in the research literature, it is difficult to determine the best method of controlling for cohort differences.
However, it is worth reiterating that I was not claiming that cohort differences are not a potentially important
determinant of the discrepancy between cross-sectional and
longitudinal age trends, but rather was suggesting that
until the relevant characteristics are identified and measured to allow their influences to be evaluated, the cohort
concept runs the risk of not being scientifically meaningful.
Another point in the commentary is that in addition to
practice effects, short-term retest effects reflect fluctuation
of an individual’s observed score around his/her true score. I
agree with this point, but I also assume that this type of fluctuation of an observed score around the true score operates
at all measurement occasions, including those separated by
long intervals in traditional longitudinal studies. It isn’t clear
from his commentary whether Schaie assumes that fluctuations around the true score do not occur with longer retest
T.A. Salthouse / Neurobiology of Aging 30 (2009) 530–533
intervals, but only if this were the case would this objection
affect the interpretation of the short-term retest effects.
As with Nilsson et al. (this issue), Schaie claims that one
particular method of assessing practice effects is “generally
accepted,” and that it was not done in the target article.
Because several other methods have recently been used
to investigate retest effects, and because the twice-versusonce-tested method has limitations such as the difficulty of
evaluating statistical significance of the retest effects and
the inability to examine relations of retest effects with other
variables, I do not believe that there is currently a consensus regarding the best method of distinguishing retest and
maturation effects. Furthermore, it should be noted that the
target article reported results with three analytical methods,
including the twice-versus-once tested method.
In his final comment, Schaie questions the power to
detect significant correlations with the retest interval variable
because of small N’s. It is certainly possible that some relations were not detected because of low power, but it should be
pointed out that the correlations between the retest interval
and the size of the longitudinal change score were signifi-
533
cant for some cognitive variables but not for others, and yet
they all had the same sample sizes. Furthermore, an earlier
study found similar estimates of long decay rates for retest
effects with different variables and samples of participants
(Salthouse et al., 2004).
In conclusion, I want to thank the reviewers for their
thoughtful comments on the target article. Exchanges such as
these can be very valuable in two respects. First, they serve
to clarify points of disagreement and thereby might stimulate
future research. And second, it can be argued that progress
in science occurs by constant questioning, not only of new
research findings, but also of long held, “widely established”
and “generally accepted” assumptions.
References
Salthouse, T.A., in press. Major issues in cognitive aging. Oxford University
Press, New York.
Salthouse, T.A., Schroeder, D.H., Ferrer, E., 2004. Estimating retest effects
in longitudinal assessments of cognitive functioning in adults between
18 and 60 years of age. Developmental Psychology 40, 813–822.
Download